Anaerobic degradation of aromatic compounds coupled to Fe(III) reduction by Ferroglobus placidus

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Anaerobic benzene oxidation coupled to the reduction of Fe(III) was studied inFerroglobus placidusin order to learn more about how such a stable molecule could be metabolized under strict anaerobic conditions.F. placidusconserved energy to support growth at 85°C in a medium with benzene provided as the sole electron donor and Fe(III) as the sole electron acceptor. The stoichiometry of benzene loss and Fe(III) reduction, as well as the conversion of [14C]benzene to [14C]carbon dioxide, was consistent with complete oxidation of benzene to carbon dioxide with electron transfer to Fe(III). Benzoate, but not phenol or toluene, accumulated at low levels during benzene metabolism, and [14C]benzoate was produced from [14C]benzene. Analysis of gene transcript levels revealed increased expression of genes encoding enzymes for anaerobic benzoate degradation during growth on benzene versus growth on acetate, but genes involved in phenol degradation were not upregulated during growth on benzene. A gene for a putative carboxylase that was more highly expressed in benzene- than in benzoate-grown cells was identified. These results suggest that benzene is carboxylated to benzoate and that phenol is not an important intermediate in the benzene metabolism ofF. placidus. This is the first demonstration of a microorganism in pure culture that can grow on benzene under strict anaerobic conditions and for which there is strong evidence for degradation of benzene via clearly defined anaerobic metabolic pathways. Thus,F. placidusprovides a much-needed pure culture model for further studies on the anaerobic activation of benzene in microorganisms.

Section: Resultsmentioning

confidence: 45%

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confidence: 99%

Anaerobic Oxidation of Benzene by the Hyperthermophilic Archaeon Ferroglobus placidus

Holmes

Risso

Smith

et al. 2011

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“…Ferroglobus placidus medium was prepared as previously described (27). After autoclaving, FeCl 2 (1.3 mM), Na 2 SeO 4 (30 g/liter), Na 2 WO 4 (40 g/liter), APM salts (1 g/liter MgCl 2 , 0.23 g/liter CaCl 2 ) (28), DL vitamins (29), and all electron donors were added to the sterilized medium from anaerobic stock solutions.…”

Section: Methodsmentioning

confidence: 99%

Mechanisms Involved in Fe(III) Respiration by the Hyperthermophilic Archaeon Ferroglobus placidus

Smith

Aklujkar

Risso

et al. 2015

The hyperthermophilic archaeon Ferroglobus placidus can utilize a wide variety of electron donors, including hydrocarbons and aromatic compounds, with Fe(III) serving as an electron acceptor. In Fe(III)-reducing bacteria that have been studied to date, this process is mediated by c-type cytochromes and type IV pili. However, there currently is little information available about how this process is accomplished in archaea. In silico analysis of the F. placidus genome revealed the presence of 30 genes coding for putative c-type cytochrome proteins (more than any other archaeon that has been sequenced to date), five of which contained 10 or more heme-binding motifs. When cell extracts were analyzed by SDS-PAGE followed by heme staining, multiple bands corresponding to c-type cytochromes were detected. Different protein expression patterns were observed in F. placidus cells grown on soluble and insoluble iron forms. In order to explore this result further, transcriptomic studies were performed. Eight genes corresponding to multiheme c-type cytochromes were upregulated when F. placidus was grown with insoluble Fe(III) oxide compared to soluble Fe(III) citrate as an electron acceptor. Numerous archaella (archaeal flagella) also were observed on Fe(III)-grown cells, and genes coding for two type IV pilin-like domain proteins were differentially expressed in Fe(III) oxidegrown cells. This study provides insight into the mechanisms for dissimilatory Fe(III) respiration by hyperthermophilic archaea.

“…Only one other thermophilic Fe(III) reducer, D. thermophilus, has this type of metabolism. The ability to use acetate is an important physiological factor for competing in anaerobic environments, since acetate is a key intermediate in the anaerobic degradation of organic matter in sedimentary environments (28,55,56). Most previously described thermophilic Fe(III) reducers do not use acetate and only incompletely oxidize other multicarbon organic acid substrates to acetate (27).…”

Section: Discussionmentioning

confidence: 99%

“…Novel hyperthermophiles with Fe(III) serving as the electron acceptor have been isolated (19,21), and it has been shown that the metabolic potential of some previously described hyperthermophiles is significantly enhanced when Fe(III) is provided as an electron acceptor (56,57). Studies with Fe(III)-reducing hyperthermophiles have documented for the first time the potential for the oxidation of important organic compounds, such as acetate, long-chain fatty acids, and aromatic compounds, in environments hotter than 80°C (21,55,56).…”

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confidence: 99%

Thermophily in the Geobacteraceae : Geothermobacter ehrlichii gen. nov., sp. nov., a Novel Thermophilic Member of the Geobacteraceae from the “Bag City” Hydrothermal Vent

Kashefi

Holmes

Baross

et al. 2003

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Little is known about the microbiology of the “Bag City” hydrothermal vent, which is part of a new eruption site on the Juan de Fuca Ridge and which is notable for its accumulation of polysaccharide on the sediment surface. A pure culture, designated strain SS015, was recovered from a vent fluid sample from the Bag City site through serial dilution in liquid medium with malate as the electron donor and Fe(III) oxide as the electron acceptor and then isolation of single colonies on solid Fe(III) oxide medium. The cells were gram-negative rods, about 0.5 μm by 1.2 to 1.5 μm, and motile and contained c-type cytochromes. Analysis of the 16S ribosomal DNA (rDNA) sequence of strain SS015 placed it in the family Geobacteraceae in the delta subclass of the Proteobacteria. Unlike previously described members of the Geobacteraceae, which are mesophiles, strain SS015 was a thermophile and grew at temperatures of between 35 and 65°C, with an optimum temperature of 55°C. Like many previously described members of the Geobacteraceae, strain SS015 grew with organic acids as the electron donors and Fe(III) or nitrate as the electron acceptor, with nitrate being reduced to ammonia. Strain SS015 was unique among the Geobacteraceae in its ability to use sugars, starch, or amino acids as electron donors for Fe(III) reduction. Under stress conditions, strain SS015 produced copious quantities of extracellular polysaccharide, providing a model for the microbial production of the polysaccharide accumulation at the Bag City site. The 16S rDNA sequence of strain SS015 was less than 94% similar to the sequences of previously described members of the Geobacteraceae; this fact, coupled with its unique physiological properties, suggests that strain SS015 represents a new genus in the family Geobacteraceae. The name Geothermobacter ehrlichii gen. nov., sp. nov., is proposed (ATCC BAA-635 and DSM 15274). Although strains of Geobacteraceae are known to be the predominant Fe(III)-reducing microorganisms in a variety of Fe(III)-reducing environments at moderate temperatures, strain SS015 represents the first described thermophilic member of the Geobacteraceae and thus extends the known environmental range of this family to hydrothermal environments.